Environmental quality predicts optimal egg size in the wild

American Naturalist

Volumn 182, Issue 1, 2013, Pages 76-90

  Rollinson, Njal ^a   Hutchings, Jeffrey A ^a,b  

^a DALHOUSIE UNIVERSITY   (Canada)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

Body size; Environmental variation; Fitness function; Investment per offspring; Minimum viable offspring size; Parental care

Indexed keywords

BODY SIZE; EGG SIZE; ENVIRONMENTAL GRADIENT; ENVIRONMENTAL QUALITY; FECUNDITY; FITNESS; HABITAT QUALITY; PARENTAL CARE; REPRODUCTIVE COST; REPRODUCTIVE SUCCESS; SALMONID; STREAMWATER; SURVIVAL; TRADE-OFF; WILD POPULATION;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CANADA; ECOSYSTEM; EVOLUTION; GENETIC SELECTION; GROWTH, DEVELOPMENT AND AGING; OOCYTE; PHYSIOLOGY; REPRODUCTION; REPRODUCTIVE FITNESS; RIVER; SALMON;

ANIMALS; BIOLOGICAL EVOLUTION; ECOSYSTEM; GENETIC FITNESS; MODELS, BIOLOGICAL; NOVA SCOTIA; OVUM; REPRODUCTION; RIVERS; SALMON; SELECTION, GENETIC;

SALMO SALAR;

EID: 84879180110     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/670648     Document Type: Article

References (86)

1. Achord, S., P. S. Levin, and R. W. Zabel. 2003. Density-dependent mortality in Pacific salmon: the ghost of impacts past? Ecology Letters 6:335-342.
2. Armstrong, J. D., and K. H. Nislow. 2006. Special section critical habitat during the transition from maternal provisioning in freshwater fish, with emphasis on Atlantic salmon (Salmo salar) and brown trout (Salmo trutta). Journal of Zoology 269:403-413.
3. Bailey, M. M., and M. T. Kinnison. 2010. Habitat-mediated size selection in endangered Atlantic salmon fry: selectional restoration assessment. Evolutionary Applications 3:352-362.
4. Bashey, F. 2008. Competition as a selective mechanism for larger offspring size in guppies. Oikos 117:104-113.
5. Bjornn, T. C., and D. W. Reiser. 1991. Habitat requirements of salmonids in streams. American Fisheries Society Special Publication 19:83-138.
6. Bohlin, T., S. Hamrin, T. Heggberget, G. Rasmussen, and S. Saltveit. 1989. Electrofishing: theory and practice with special emphasis on salmonids. Hydrobiologia 173:9-43.
7. Bonabeau, E., J.-L. Deneubourg, and G. Theraulaz. 1998. Withinbrood competition and the optimal partitioning of parental investment. American Naturalist 153:419-427.
8. Boudreault, A. 1984. Méthodologie utilisée pour la photo-interprétation des rivières à saumon de la Côte-Nord. Rapport réalisé par Gilles Shooner Inc. pour le Ministère du Loisir, de la Chasse et de la Pêche, Direction de la faune aquatique. Loretteville, Quebec.
9. Bujold, V., R. A. Cunjak, J. P. Dietrich, and D. A. Courtemanche. 2004. Drifters versus residents: assessing size and age differences in Atlantic salmon (Salmo salar) fry. Canadian Journal of Fisheries and Aquatic Sciences 282:273-282.
10. Burnham, K. P., and D. R. Anderson. 2002. Model selection and multimodel inference: a practical information-theoretic approach. 2nd ed. Springer, New York.
11. Charpentier, A., M. Anand, and C. T. Bauch. 2012. Variable offspring size as an adaptation to environmental heterogeneity in a clonal plant species: integrating experimental and modelling approaches. Journal of Ecology 100:184-195.
12. Dias, G. M., and D. J. Marshall. 2010. Does the relationship between offspring size and performance change across the life-history? Oikos 119:154-162.
13. Einum, S., A. G. Finstad, G. Robertsen, K. H. Nislow, S. McKelvey, and J. D. Armstrong. 2011. Natal movement in juvenile Atlantic salmon: a body size-dependent strategy? Population Ecology 54: 285-294.
14. Einum, S., and I. A. Fleming. 1999. Maternal effects of egg size in brown trout (Salmo trutta): norms of reaction to environmental quality. Proceedings of the Royal Society B: Biological Sciences 266:2095-2100.
15. Einum, S., and I. A. Fleming. 2000a. Highly fecund mothers sacrifice offspring survival to maximize fitness. Nature 405:565-567.
16. Einum, S., and I. A. Fleming. 2000b. Selection against late emergence and small offspring in Atlantic salmon (Salmo salar). Evolution 54:628-639.
17. Einum, S., and I. A. Fleming. 2002. Does within-population variation in fish egg size reflect maternal influences on optimal values? American Naturalist 160:756-765.
18. Einum, S., and I. A. Fleming. 2004. Environmental unpredictability and offspring size: conservative versus diversified bet-hedging. Evolutionary Ecology Research 6:443-455.
19. Einum, S., A. P. Hendry, and I. A. Fleming. 2002. Egg-size evolution in aquatic environments: does oxygen availability constrain size? Proceedings of the Royal Society B: Biological Sciences 269:2325-2330.
20. Einum, S., and K. H. Nislow. 2005. Local-scale density-dependent survival of mobile organisms in continuous habitats: an experimental test using Atlantic salmon. Oecologia (Berlin) 143:203-210.
21. Elliott, J., and M. A. Hurley. 1997. A functional model for maximum growth of Atlantic salmon parr, Salmo salar, from two populations in northwest England. Functional Ecology 11:592-603.
22. Erös, T., P. Gustafsson, L. A. Greenberg, and E. Bergman. 2012. Forest-stream linkages: effects of terrestrial invertebrate input and light on diet and growth of brown trout (Salmo trutta) in a boreal forest stream. PloS ONE 7:e36462.
23. Finstad, A. G., S. Einum, T. Forseth, and O. Ugedal. 2007. Shelter availability affects behaviour, size-dependent and mean growth of juvenile Atlantic salmon. Freshwater Biology 52:1710-1718.
24. Finstad, A. G., S. Einum, O. Ugedal, and T. Forseth. 2009. Spatial distribution of limited resources and local density regulation in juvenile Atlantic salmon. Journal of Animal Ecology 78:226-35.
25. Fox, C., M. Thakar, and T. Mousseau. 1997. Egg size plasticity in a seed beetle: an adaptive maternal effect. American Naturalist 149: 149-193.
26. Fraser, D. J., M. W. Jones, T. L. McParland, and J. A. Hutchings. 2007. Loss of historical immigration and the unsuccessful rehabilitation of extirpated salmon populations. Conservation Genetics 8:527-546.
27. Fuller, R. L., C. LaFave, M. Anastasi, J. Molina, H. Salcedo, and S. Ward. 2007. The role of canopy cover on the recovery of periphyton and macroinvertebrate communities after a month-long flood. Hydrobiologia 598:47-57.
28. Guay, J. C., D. Boisclair, D. Rioux, M. Leclerc, M. Lapointe, and P. Legendre. 2000. Development and validation of numerical habitat models for juveniles of Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences 57:2065-2075.
29. Hedger, D. R., J. J. Dodson, N. E. Bergeron, and F. Caron. 2005. Habitat selection by juvenile Atlantic salmon: the interaction between physical habitat and abundance. Journal of Fish Biology 67: 1054-1071.
30. Heggenes, J. 1988. Substrate preferences of brown trout fry (Salmo trutta) in artificial stream channels. Canadian Journal of Fisheries and Aquatic Sciences 45:1801-1806.
31. Hendry, A. P., T. Day, and A. B. Cooper. 2001. Optimal size and number of propagules: allowance for discrete stages and effects of maternal size on reproductive output and offspring fitness. American Naturalist 157:387-407.
32. Houde, A. L. S., D. J. Fraser, P. O'Reilly, and J. A. Hutchings. 2011a. Maternal and paternal effects on fitness correlates in outbred and inbred Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences 68:534-549.
33. Houde, A. L. S., D. J. Fraser, P. O'Reilly, and J. A. Hutchings. 2011b. Relative risks of inbreeding and outbreeding depression in the wild in endangered salmon. Evolutionary Applications 4:634-647.
34. Hurlbert, S. H. 1984. Pseudoreplication and the design of ecological field experiments. Ecological Monographs 54:187-211.
35. Hutchings, J. A. 1991. Fitness consequences of variation in egg size and food abundance in brook trout Salvelinus fontinalis. Evolution 45:1162-1168.
36. Hutchings, J. A. 1997. Life history responses to environmental variability in early life. Pages 139-168 in R. C. Chambers and E. A. Trippel, eds. Early life history and recruitment in fish populations. Chapman & Hall, London.
37. Jaeger, R. G. 1981. Dear enemy recognition and the costs of aggression between salamanders. American Naturalist 117:962-974.
38. Johnson, D. W., M. R. Christie, and J. Moye. 2010. Quantifying evolutionary potential of marine fish larvae: heritability, selection, and evolutionary constraints. Evolution 64:2614-2628.
39. Johnston, T. A., and W. C. Leggett. 2002. Maternal and environmental gradients in the egg size of an iteroparous fish. Ecology 83:1777-1791.
40. Kamler, E. 2006. Parent-egg-progeny relationships in teleost fishes: an energetics perspective. Reviews in Fish Biology and Fisheries 15:399-421.
41. Kane, T. R. 1988. Relationship of temperature and time of initial feeding of Atlantic salmon. Progressive Fish-Culturist 50:93-97.
42. Kvingedal, E., and S. Einum. 2011. Prior residency advantage for Atlantic salmon in the wild: effects of habitat quality. Behavioral Ecology and Sociobiology 65:1295-1303.
43. Lack, D. 1947. The significance of clutch-size. Ibis 89:302-352.
44. Lande, R., and S. J. Arnold. 1983. The measurement of selection on correlated characters. Evolution 37:1210-1226.
45. Levin, P. S., S. Achrod, B. E. Feist, and R. W. Zabel. 2002. Nonindigenous brook trout and the demise of Pacific salmon: a forgotten threat? Proceedings of the Royal Society B: Biological Sciences 269:1663-1670.
46. Marshall, D. J., and T. F. Bolton. 2007. Effects of egg size on the development time of non-feeding larvae. Biological Bulletin 212: 6-11.
47. Marshall, D. J., and M. J. Keough. 2008. The relationship between offspring size and performance in the sea. American Naturalist 171:214-224.
48. Marshall, D. J., and M. J. Keough. 2009. Does interspecific competition affect offspring provisioning? Ecology 90:487-495.
49. McGinley, M. A., D. H. Temme, and M. A. Geber. 1987. Parental investment in offspring in variable environments: theoretical and empirical considerations. American Naturalist 130:370-398.
50. Mebane, C. A. 2001. Testing bioassessment metrics: macroinvertebrate, sculpin, and salmonid responses to stream habitat, sediment, and metals. Environmental Monitoring and Assessment 67:293-322.
51. Millidine, K. J., J. D. Armstrong, and N. B. Metcalfe. 2006. Presence of shelter reduces maintenance metabolism of juvenile salmon. Functional Ecology 20:839-845.
52. Murphy, M. L., J. Heifetz, S. W. Johnson, K. V. Koski, and J. F. Thedinga. 1986. Effects of clear-cut logging with and without buffer strips on juvenile salmonids in Alaskan streams. Canadian Journal of Fisheries and Aquatic Sciences 43:1521-1533.
53. Mäki-Petays, A., A. Huusko, J. Erkinaro, and T. Muotka. 2002. Transferability of habitat suitability criteria of juvenile Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences 59:218-228.
54. Nakano, S., and M. Murakami. 2001. Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. Proceedings of the National Academy of Sciences of the USA 98:166-170.
55. Nislow, K. H., S. Einum, and C. L. Folt. 2004. Testing predictions of the critical period for survival concept using experiments with stocked Atlantic salmon. Journal of Fish Biology 65(suppl. 1):188-200.
56. Nislow, K. H., C. L. Folt, and D. L. Parrish. 1999. Favorable foraging locations for young Atlantic salmon: application to habitat and population restoration. Ecological Applications 9:1085-1099.
57. Olofsson, H., J. Ripa, and N. Jonzén. 2009. Bet-hedging as an evolutionary game: the trade-off between egg size and number. Proceedings of the Royal Society B: Biological Sciences 276:2963-2969.
58. Ostrovsky, I. 1995. The parabolic pattern of animal growth: determination of equation parameters and their temperature dependencies. Freshwater Biology 33:357-371.
59. O'Grady, M. F. 1993. Initial observations on the effects of varying levels of deciduous bankside vegetation on salmonid stocks in Irish waters. Aquaculture and Fisheries Management 24:563-573.
60. O'Reilly, P. T., and C. J. Harvie. 2009. Conservation of genetic variation in the inner Bay of Fundy Atlantic salmon captive breeding and rearing program. Canadian Science Advisory Secretariat Research Document 2009/095. Department of Fisheries and Oceans, Dartmouth, Nova Scotia.
61. Parker, G. A., and M. Begon. 1986. Optimal egg size and clutch size: effects of environment and maternal phenotype. American Naturalist 128:573-592.
62. Pepin, P., D. C. Orr, and J. T. Anderson. 1997. Time to hatch and larval size in relation to temperature and egg size in Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 54(suppl. 1):2-10.
63. Purchase, C., and J. Hutchings. 2008. A temporally stable spatial pattern in the spawner density of a freshwater fish: evidence for an ideal despotic distribution. Canadian Journal of Fisheries and Aquatic Sciences 65:382-388.
64. R Development Core Team. 2012. R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. http://www.R-project.org,.
65. Rees, M., and L. D. Venable. 2007. Why do big plants make big seeds? Journal of Ecology 95:926-936.
66. Riddick, E. W., and Z. Wu. 2012. Mother-offspring relations: prey quality and maternal size affect egg size of an acariphagous lady beetle in culture. Psyche: A Journal of Entomology 2012:1-7.
67. Riley, W. D., M. G. Pawson, V. Quayle, and M. J. Ives. 2009. The effects of stream canopy management on macroinvertebrate communities and juvenile salmonid production in a chalk stream. Fisheries Management and Ecology 16:100-111.
68. Ritz, C., and J. Strebig. 2011. drc: analysis of dose-response curves. Retrieved from http://cran.r-project.org/.
69. Rollinson, N., and J. A. Hutchings. 2010. Why does egg size increase with maternal size? effects of egg size and egg density on offspring phenotypes in Atlantic salmon (Salmo salar). Evolutionary Ecology Research 12:949-960.
70. Rollinson, N., and J. A. Hutchings. 2011a. Body size-specific maternal effects on the offspring environment shape juvenile phenotypes in Atlantic salmon. Oecologia (Berlin) 166:889-898.
71. Rollinson, N., and J. A. Hutchings. 2011b. Why does egg size of salmonids increase with the mean size of population spawning gravels? Canadian Journal of Fisheries and Aquatic Sciences 68:1307-1315.
72. Rollinson, N., and J. A. Hutchings. 2013. The relationship between offspring size and fitness: integrating theory and empiricism. Ecology 94:315-324.
73. Rollinson, N., R. G. Farmer, and R. J. Brooks. 2012. Widespread reproductive variation in North American turtles: temperature, egg size and optimality. Zoology 115:160-169.
74. Rombough, P. J. 2007. Oxygen as a constraining factor in egg size evolution in salmonids. Canadian Journal of Fisheries and Aquatic Sciences 64:692-699.
75. Sinervo, B., K. Zamudio, P. Doughty, and R. B. Huey. 1992. Allometric engineering: a causal analysis of natural selection on offspring size. Science 258:1927-1930.
76. Smith, C., and S. Fretwell. 1974. The optimal balance between size and number of offspring. American Naturalist 108:499-506.
77. Steingrimsson, S. O., and J.W. A. Grant. 2003. Patterns and correlates of movement and site fidelity in individually-tagged young-of-theyear Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences 60:193-202.
78. Suttle, K. B., M. E. Power, J. M. Levine, and C. McNeely. 2004. How fine sediment in riverbeds impairs growth and survival of juvenile salmonids. Ecological Applications 14:969-974.
79. Svärdson, G. 1949. Natural selection and egg number in fish. Pages 115-122 in Report 29. Institute of Freshwater Research, Drottningholm, Sweden.
80. Svensson, E., and B. Sinervo. 2000. Experimental excursions on adaptive landscapes: density-dependent selection on egg size. Evolution 54:1396-1403.
81. Taborsky, B. 2006. Mothers determine offspring size in response to own juvenile growth conditions. Biology Letters 2:225-228.
82. Tymchuk, W. V., P. O'Reilly, J. Bittman, D. Macdonald, and P. Schulte. 2010. Conservation genomics of Atlantic salmon: variation in gene expression between and within regions of the Bay of Fundy. Molecular Ecology 19:1842-1859.
83. Vehanen, T. 2003. Adaptive flexibility in the behaviour of juvenile Atlantic salmon: short-term responses to food availability and threat from predation. Journal of Fish Biology 63:1034-1045.
84. Webb, J. H., R. J. Fryer, J. B. Taggart, C. E. Thompson, and A. F. Youngson. 2001. Dispersion of Atlantic salmon (Salmo salar) fry from competing families as revealed by DNA profiling. Canadian Journal of Fisheries and Aquatic Sciences 58:2386-2395.
85. Zar, J. H. 1984. Biostatistical analysis. 2nd ed. Prentice-Hall, London.
86. Zimmermann, E. M., and R. G. Death. 2002. Effect of substrate stability and canopy cover on stream invertebrate communities. New Zealand Journal of Marine and Freshwater Research 36:537-545.